Abstract
Louping ill virus (LIV) is a tick-borne flavivirus that is part of the tick-borne encephalitis complex of viruses (TBEV) and has economic and welfare importance by causing illness and death in livestock, especially sheep, Ovies aries, and red grouse, Lagopus lagopus scoticus, an economically valuable gamebird. Unlike Western TBEV which is found primarily in woodlands and is reservoired by small rodents, LIV is not generally transmitted by small rodents but instead by sheep, red grouse and mountain hares and, therefore, is associated with upland heather moorland and rough grazing land. Red grouse are a particularly interesting transmission host because they may acquire most of their LIV infections through eating ticks rather than being bitten by ticks. Furthermore, the main incentive for the application of LIV control methods is not to protect sheep, but to protect red grouse, which is an economically important gamebird. The widespread intensive culling of mountain hares which has been adopted in several areas of Scotland to try to control ticks and LIV has become an important issue in Scotland in recent years. This review outlines the reservoir hosts and transmission cycles of LIV in the UK, then describes the various control methods that have been tried or modelled, with far-reaching implications for conservation and public opinion.
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References
Balseiro A, Royo LJ, Martínez CP, Fernández de Mera IG, Höfle Ú, Polledo L, Marreros N, Casais R, Marín JF (2012) Louping ill in goats, Spain, 2011. Emerg Infect Dis 18:976–978
Beasley SJ, Campbell JA, Reid HW (1978) Threshold problems in infection in Ixodes ricinus with the virus of louping-ill. In: Wild JKH (ed) Tick-borne diseases and their vectors. Edinburgh University Press, Edinburgh, pp 497–500
Brei B, Brownstein JS, George JE, Pound JM, Miller JA, Daniels TJ, Falco RC, Stafford KC, Schulze TL, Mather TN, Carroll JF, Fish D (2009) Evaluation of the United States department of agriculture northeast area-wide tick control project by meta-analysis. Vector Borne Zoonotic Dis 9:423–430
Gao GF, Jiang WR, Hussain MH, Venugopal K, Gritsun TS, Reid HW, Gould EA (1993) Sequencing and antigenic studies of a Norwegian virus isolated from encephalomyelitic sheep confirm the existence of louping ill virus outside Great Britain and Ireland. J Gen Virol 74:109–114
Gao GF, Hussian MH, Reid HW, Gould EA (1994) Identification of naturally occurring monoclonal antibody escape variants of louping ill virus. J Gen Virol 75:609–614
Gao GF, Zanotto PM, Holmes EC, Reid HW, Gould EA (1997) Molecular variation, evolution and geographical distribution of louping ill virus. Acta Virol 41:259–268
Gaunt MW (1997) The epidemiology of louping ill virus and flavivirus evolution. PhD Thesis, University of Oxford, UK
Gilbert L, Jones LD, Hudson PJ, Gould EA, Reid HW (2000) The role of small mammals in the persistence of louping-ill virus: field survey and co-feeding studies. Med Vet Entomol 14:78–283
Gilbert L, Norman R, Laurenson KM, Reid HW, Hudson PJ (2001) Disease persistence and apparent competition in a three-host community: an empirical and analytical study of large scale wild populations. J Anim Ecol 70:1053–1061
Gilbert L, Jones LD, Laurenson MK, Gould EA, Reid HW, Hudson PJ (2004) Ticks need not bite their red grouse hosts to infect them with louping ill virus. Proc R Soc Lond B Suppl Biol Lett 271:S202–S205
Gilbert L, Maffey GL, Ramsay SL, Hester AJ (2012) The effect of deer management on the abundance of Ixodes ricinus in Scotland. Ecol Apps 22:658–667
Gonzalez L, Reid HW, Pow I, Gilmour JS (1987) A disease resembling louping-ill in sheep in the Basque region of Spain. Vet Rec 121:12–13
Grard G, Moureau G, Charrel RN, Lemasson J-J, Gonzalez J-P, Gallian P, Gritsun TS, Holmes EC, Gould EA, de Lamballerie X (2007) Genetic characterization of tick-borne flaviviruses: new insights into evolution, pathogenetic determinants and taxonomy. Virology 361:80–92
Gray JS (1998) The ecology of ticks transmitting Lyme borreliosis. Exp Appl Acarol 22:249–258
Gritsun TS, Lashkevich VA, Gould EA (2003) Tick-borne encephalitis. Antivir Res 57:129–146
Harrison AK (2011) Dispersal and compensatory population dynamics in a harvested mammal. PhD Thesis, University of Glasgow, UK
Harrison A, Newey S, Gilbert L, Haydon DT, Thirgood SJ (2010) Culling wildlife hosts to control disease: mountain hares, red grouse and louping ill virus. J Appl Ecol 47:926–930
Hoen AG, Rollend LG, Papero MA, Carroll JF, Daniels TJ, Mather TN, Schulze TL, Stafford KCIII, Fish D (2009) Effects of tick control by acaricide self-treatment of white-tailed deer on host-seeking tick infection prevalence and entomological risk for Ixodes scapularis-borne-pathogens. Vector Borne Zoonotic Dis 9:431–438
Hudson PJ (1986) Red grouse: the biology and management of a wild gamebird. The Game Conservancy Trust, Fordingbridge
Hudson PJ, Norman R, Laurenson MK, Newborn D, Gaunt M, Jones LD, Reid HW, Gould EA, Bowers R, Dobson A (1995) Persistence and transmission of tick-borne viruses: Ixodes ricinus and louping ill virus in red grouse populations. Parasitology 111:S49–S58
Jeffries CL, Mansfield KL, Phipps LP, Wakeley PR, Mearns R, Schock A, Bell S, Breed AC, Fooks AR, Johnson N (2014) Louping ill virus: an endemic tick-borne disease of Great Britain. Virology 95:1005–1014
Jensen PM, Skarphedinsson S, Semenov A (2004) Densities of the tick (Ixodes ricinus) and coexistence of the louping ill virus and tick borne encephalitis virus on the island of Bornholm. Ugeskr Laeg 166:2563–2565 (in Danish)
Jones L, Gaunt M, Hails R, Laurenson K, Hudson PJ, Reid HW, Gould E (1997) Amplification of louping-ill virus infection during co-feeding of ticks on mountain hares (Lepus timidus). Med Vet Entomol 11:172–176
Jones E, Webb SD, Ruiz-Fons F, Albon S, Gilbert L (2011) The effect of landscape heterogeneity and host movement on a tick-borne pathogen. Theor Ecol 4:435–448
Kiffner C, Lödige C, Alings M, Vor T, Rühe F (2010) Abundance estimation of Ixodes ticks (Acari: Ixodidae) on roe deer (Capreolus capreolus). Exp Appl Acarol 52:73–84
Labuda M, Nuttall PA, Kozuch O, Eleckova E, Williams T, Zuffová E, Sabó A (1993) Nonviraemic transmission of tick-borne encephalitis virus: a mechanism for arbovirus survival in nature. Experientia 49:802–805
Labuda M, Kozuch O, Zuffova E, Eleckova E, Hails RS, Nuttall PA (1997) Tick-borne encephalitis virus transmission between ticks cofeeding on specific immune natural rodent hosts. Virology 235:138–143
Laurenson MK, Hudson PJ, McGuire K, Thirgood SJ, Reid HW (1997) Efficacy of acaricidal tags and pour-on as prophylaxis against ticks and louping-ill in red grouse. Med Vet Entomol 11:389–393
Laurenson MK, Norman RA, Gilbert L, Reid HW, Hudson PJ (2003) Identifying disease reservoirs in complex systems: mountain hares as reservoirs of ticks and louping-ill virus, pathogens of red grouse. J Anim Ecol 72:177–185
Laurenson MK, McKendrick IJ, Reid HW, Challenor R, Mathewson GK (2007) Prevalence, spatial distribution and the effect of control measures on louping-ill virus in the Forest of Bowland, Lancashire. Epidemiol Infect 135:963–973
McGuire K, Homes EC, Gao GF, Reid HW, Gould EA (1998) Tracing the origins of louping ill virus by molecular phylogenetic analysis. J Gen Virol 79:981–988
Mougeot F, Moseley M, Leckie F, Martinez-Padilla J, Miller A, Pounds N, Irvine RJ (2008) Reducing tick burdens on chicks by treating breeding female grouse with permethrin. J Wildl Manag 72:468–472
Mysterud A, Hatlegjerde IL, Sørensen OJ (2015) Attachment site selection of life stages of Ixodes ricinus ticks on a main large host in Europe, the red deer (Cervus elaphus). Parasit Vectors 7:510
Newborn D, Baines D (2012) Enhanced control of sheep ticks in upland sheep flocks: repercussions for red grouse co-hosts. Med Vet Entomol 26:63–69
Ogden NH, Hailes RS, Nuttal PA (1998) Interstadial variation in the attachment sites of Ixodes ricinus ticks on sheep. Exp Appl Acarol 22:227–232
Park KJ, Robertson PA, Campbell ST, Foster R, Russell ZM, Newborn D, Hudson PJ (2001) The role of invertebrates in the diet, growth and survival of red grouse (Lagopus lagopus scoticus) chicks. J Zool 254:137–145
Porter R, Norman R, Gilbert L (2011) Controlling tick borne diseases through domestic animal management: a theoretical approach. Theor Ecol 4:321–339
Porter R, Norman R, Gilbert L (2013a) A model to test how ticks and louping ill virus can be controlled by treating red grouse with acaricide. Med Vet Entomol 27:237–246
Porter R, Norman R, Gilbert L (2013b) An alternative to killing? Treating wildlife hosts to protect a valuable species from a shared parasite. Parasitology 140:247–257
Reid HW (1975) Experimental infection of the red grouse with louping-ill virus (Flavivirus group). I. The viraemia and antibody response. J Comp Pathol 85:231–235
Reid HW (1978) The epidemiology of louping-ill. In: Wild JKH (ed) Tick-borne diseases and their vectors. Edinburgh University Press, Edinburgh, pp 501–507
Reid HW (1984) Epidemiology of louping-ill. In: Mayo MA, Harrap KA (eds) Vectors in biology. Academic Press, London, pp 161–178
Reid HW (1988) Louping ill. In: Monat TB (ed) The arboviruses: epidemiology and ecology, vol 3. CRC Press, Boca Raton, pp 117–135
Reid HW, Doherty PC (1971) Experimental louping-ill in sheep and lambs 1. Viraemia and the antibody response. J Comp Pathol 81:291–298
Reid HW, Moss R (1980) The response of four species of birds to louping ill virus. Zent Bakt Parasit Infektion Hyg 1(Abt Suppl 9):220–223
Reid HW, Barlow RM, Boyce JB, Inglis DM (1976) Isolation of louping-ill virus from a roe deer (Capreolus capreolus). Vet Rec 98:116
Reid HW, Barlow RM, Pow I, Maddox J (1978a) Isolation of louping-ill virus from a red deer (Cervus elaphus). Vet Rec 102:463–464
Reid HW, Duncan JS, Phillips J, Moss R, Watson A (1978b) Studies on louping-ill virus (Flavivirus group) in wild red grouse (Lagopus lagopus scoticus). J Hyg 8:321–329
Reid HW, Moss R, Pow I (1980) The response of three grouse species (Tetrao urogallus, Lagopus mutus, Lagopus lagopus) to louping-ill virus. J Comp Path 90:257–263
Reid HW, Buxton D, Pow I, Moss R (1983) Experimental louping-ill virus infection of black grouse (Tetrao tetrix). Arch Virol 78:299–302
Rizzoli A, Hauffe HC, Tagliapietra V, Neteler M, Rosá R (2009) Forest structure and roe deer abundance predict tick-borne encephalitis risk in Italy. PLoS ONE 4:e4336
Ruiz-Fons F, Gilbert L (2010) The role of deer (Cervus elaphus and Capreolus capreolus) as vehicles to move ticks Ixodes ricinus between contrasting habitats. Int J Parasitol 40:1013–1020
Ruiz-Fons F, Fernández-de-Mera IG, Acevedo P, Gortázar C, de la Fuente J (2012) Factors driving the abundance of Ixodes ricinus ticks and the prevalence of zoonotic I. ricinus-borne pathogens in natural foci. Appl Environ Microbiol 8:2669
Ruiz-Fons F, Balseiro A, Willoughby K, Oleaga A, Dagleish MP, Pérez-Ramírez E, Havlíková S, Klempa B, Llorente F, Martín-Hernando MP (2014) Clinical infection of Cantabrian chamois (Rupicapra pyrenaica parva) by louping ill virus: new concern for mountain ungulate conservation? Eur J Wildl Res 60:691–694
Sheahan BJ, Moore M, Atkins GJ (2002) The pathogenicity of louping ill virus for mice and lambs. J Comp Pathol 126:137–146
Warren P, Baines D (2007) Dispersal distances of juvenile radiotagged red grouse Lagopus lagopus scoticus on moors in northern England. Ibis 149:758–762
Ytrehus B, Vainio K, Dudman SG, Gilray J, Willoughby K (2013) Tick-borne encephalitis virus and louping-ill virus may co-circulate in Southern Norway. Vector Borne Zoonotic Dis 13:762–768
Acknowledgments
LG was supported by the Scottish Government’s Rural and Environment Science and Analytical Services Division (RESAS). I thank Justin Irvine for useful comments on the manuscript.
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Gilbert, L. Louping ill virus in the UK: a review of the hosts, transmission and ecological consequences of control. Exp Appl Acarol 68, 363–374 (2016). https://doi.org/10.1007/s10493-015-9952-x
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DOI: https://doi.org/10.1007/s10493-015-9952-x